Environmental Evidence

Modrzejewski et al. Environ Evid (2019) 8:27 https://doi.org/10.1186/s13750-019-0171-5 Environmental Evidence SYSTEMATIC MAP Open Access What is the available evidence for the range of applications of genome-editing as a new tool for plant trait modifcation and the potential occurrence of associated of-target efects: a systematic map Dominik Modrzejewski* , Frank Hartung, Thorben Sprink, Dörthe Krause, Christian Kohl and Ralf Wilhelm Abstract Background: Within the last decades, genome-editing techniques such as CRISPR/Cas, TALENs, Zinc-Finger Nucle- ases, Meganucleases, Oligonucleotide-Directed Mutagenesis and base editing have been developed enabling a precise modifcation of DNA sequences. Such techniques provide options for simple, time-saving and cost-efective applications compared to other breeding techniques and hence genome editing has already been promoted for a wide range of plant species. Although the application of genome-editing induces less unintended modifcations (of-targets) in the genome compared to classical mutagenesis techniques, of-target efects are a prominent point of criticism as they are supposed to cause unintended efects, e.g. genomic instability or cell death. To address these aspects, this map aims to answer the following question: What is the available evidence for the range of applications of genome-editing as a new tool for plant trait modifcation and the potential occurrence of associated of-target efects? This primary question will be considered by two secondary questions: One aims to overview the market-oriented traits being modifed by genome-editing in plants and the other explores the occurrence of of-target efects. Methods: A literature search in nine bibliographic databases, Google Scholar, and 47 web pages of companies and governmental agencies was conducted using predefned and tested search strings in English language. Articles were screened on title/abstract and full text level for relevance based on pre-defned inclusion criteria. The relevant infor- mation of included studies were mapped using a pre-defned data extraction strategy. Besides a descriptive summary of the relevant literature, a spreadsheet containing all extracted data is provided. Results: Altogether, 555 relevant articles from journals, company web pages and web pages of governmental agencies were identifed containing 1328 studies/applications of genome-editing in model plants and agricultural crops in the period January 1996 to May 2018. Most of the studies were conducted in China followed by the USA. Genome- editing was already applied in 68 diferent plants. Although most of the studies were basic research, 99 diferent market-oriented applications were identifed in 28 diferent crops leading to plants with improved food and feed quality, agronomic value like growth characteristics or increased yield, tolerance to biotic and abiotic stress, herbicide tolerance or industrial benefts. 252 studies explored of-target efects. Most of the studies were conducted using CRISPR/ Cas. Several studies frstly investigated whether sites in the genome show similarity to the target sequence and secondly analyzed these potential of-target sites by sequencing. In around 3% of the analyzed potential of-target *Correspondence: [email protected] Institute for Biosafety in Plant Biotechnology, Julius Kühn-Institute, Federal Research Centre for Cultivated Plants, Erwin-Baur-Straße 27, 06484 Quedlinburg, Germany © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/ publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Modrzejewski et al. Environ Evid (2019) 8:27 Page 2 of 33 sites, unintended mutations were detected. Only a few studies conducted of-target analyses using unbiased detec- tion methods (e.g. whole genome sequencing). No of-target efects that could be correlated to the genome-editing process were identifed in these studies. Conclusions: The rapid adoption in plant breeding was demonstrated by a considerable number of market oriented applications (crops and traits) described in publications worldwide. Studies investigating of-target efects are very heterogeneous in their structure and design. Therefore, an in-depth assessment regarding their weight of evidence is mandatory. Keywords: New plant breeding techniques, Gene editing, Targeted genome modifcation, Mutagenesis, Unintended efects, Of-target mutation, Evidence map, Evidence synthesis Background meaning that yield improvement conserves the rate of Technological progress in agriculture and plant breeding land clearance, but the efect is smaller than it could be has contributed signifcantly to a stable food supply and [5]. One example for the rebound-efect in agriculture is formed the basis for high yields as well as the production the Green Revolution [6]. As a result of this revolution, of high-quality agricultural products [1]. However, in an yields increased, saving ecosystems from conversion to ever-changing world, new challenges will be encountered agricultural land. However, the efect was much smaller within the next decades. Aside the demands of the grow- than expected. One explanation for this efect may be ing global population and limited fossil resources, climate that increased productivity due to new technologies also change is a driver of breeding eforts as it is associated increases the proftability of agriculture compared with with increased extreme weather events like droughts or alternative land use [6]. foods as well as changing dynamics of pests and dis- Plant breeding essentially relies on the utilization of eases. Agriculture needs to ensure and increase the world genetic variation within the breeding material that can agricultural production to serve extended demands with be used for crossing and selection to develop improved limited environmental resources like soil and water [2]. varieties. New genetic variation occurs naturally by spon- In contrast, intensifcation of agriculture causes consid- taneous mutations that enable some individual plants in erable impact on nature, as naturally diverse landscapes a population to adapt to changing environmental con- are replaced by arable land for the cultivation of few plant ditions. However, as the mutation rate is fairly low and species. Biodiversity is threatened through habitat loss random, plant breeders and scientists have artifcially and pesticide use, which in turn is considered to increase induced mutations for several decades [7]. Te frst gen- disease and pest pressure [1]. Additionally, these impacts eration of mutation breeding used chemical and physical of agriculture on the environment are becoming increas- mutagens to generate a plurality of nonspecifc muta- ingly important in societal debates. tions. Te increased mutation rate results in plants with To meet all these challenges, improved crop varie- a few positive, a lot of neutral and several negative char- ties may be developed and integrated into a sustainable acteristics. Tus, laborious backcrossing and selection farming system considering their economic, environ- steps are necessary in order to select for a target trait in mental and social impacts [2]. Examples for a sustain- a desired genetic background (maternal variety). Never- able farming system are the preservation of natural soil theless, to date 3282 mutant varieties from 225 diferent fertility through suitable crop rotations, fertilization plant species have been generated through undirected and plant protection according to the principles of inte- mutagenesis and ofcially but voluntarily registered [8]. grated cultivation or a balanced and species-appropriate animal husbandry [3]. Additionally, plant breeding is of Glossary: [1, 9, 10] crucial importance to manage environmental impacts Backcrossing on cultivation systems by providing varieties resistant to plant diseases or pests, tolerant to abiotic stress and Backcrossing is a crossing of a hybrid with one of its more broadly support a “greener production”—in time. parents in order to achieve ofspring that are geneti- Tis may reduce pesticide use and result in less intense cally closer to the selected parent. Tis way, desired management eforts (e.g. irrigation) [4]. Further yield heterologous traits from the hybrid can be transferred improvement can increase the yield per hectare and may into the genetic background of a parental line. Since open land management options e.g. balance with areas crossing recombines all genes, many backcrosses for nature conservation [1]. Nevertheless, there is evi- are necessary to achieve considerable dilution of dence that increased yields may lead to a rebound-efect unwanted genes from the hybrid. Modrzejewski et al. Environ Evid (2019) 8:27 Page 3 of 33 Mutagen 1. No template is added and the DSB is repaired by autochthonous cellular mechanisms [in most cases A mutagen is an agent that increases the mutation non-homologous end joining (NHEJ)] resulting rate within an organism or cell, e.g. X-rays, gamma- in small insertion-deletion (indel) mutations. Tis rays or chemicals

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